the plastic plant: root responses to heterogeneous supplies of nutrients

The Plastic Plant: Root Responses to Heterogeneous Supplies of NutrientsAuthor(s): Angela HodgeSource: New Phytologist, Vol. 162, No. 1 (Apr., 2004), pp. 9-24Published by: Wiley on behalf of the New Phytologist TrustStable URL: http://www.jstor.org/stable/1514473 .

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New Phytologist Review

ansley review

The plastic plant: root responses to

heterogeneous supplies of nutrients

Author for correspondence: Angela Hodge Angela Hodge Department of Biology, Area 2, PO Box 373, University of York, York YO10 5YW, UK Tel: +44 1904 328562 Fax: +44 1904 328505 Email: [email protected]

Received: 20 August 2003

Accepted: 1 December 2003

doi: 10.1111/j.1469-8137.2004.01015.x

Contents

i. Introduction

II. Morphological responses

III. Root demography

IV. Physiological plasticity

V. Root plasticity in patches in competition and symbiosis with microorganisms

Key words: soil heterogeneity, root proliferation, root ion-uptake capacities, nutrient patches, microorganisms, patch attributes.

9 VI. Influence of patch attributes

10 VII. Control of root proliferation

14 VIII. Conclusions

17

19

20

14 Acknowledgements

References 16

20

20

Summary When roots encounter a nutrient-rich zone or patch they often proliferate within it. Roots experiencing nutrient-rich patches can also enhance their physiological ion- uptake capacities compared with roots of the same plant outside the patch zone. These plastic responses by the root system have been proposed as the major mechanism by which plants cope with the naturally occurring heterogeneous supplies of nutrients in soil. Various attempts to predict how contrasting species will respond to patches have been made based on specific root length (SRL), root demography and biomass allocation within the patch zone. No one criterion has proved definitive. Actually demonstrating that root proliferation is beneficial to the plant, especially in terms of nitrogen capture from patches, has also proved troublesome. Yet by growing plants under more realistic conditions, such as in interspecific plant competition, and with a complex organic patch, a direct benefit can be demonstrated. Thus, as highlighted in this review, the environmental context in which the root response is expressed is as important as the magnitude of the response itself.

? New Phytologist (2004) 162: 9-24

I. Introduction In soil, nutrients are distributed in a heterogeneous or patchy manner. In order to enhance resource capture, plant roots have to respond to, and exploit, these nutrient patches. This

exploitation is aided by the modular structure of the root system which enables exceptional flexibility in architectural patterns and allows root deployment in nutrient-rich zones. Physiological plasticity is also important for successful patch exploitation. These mechanisms ultimately determine the

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below-ground success of the plant, therefore it is hardly surprising they have been the focus of much research interest (see reviews by Hutchings & de Kroon, 1994; Robinson, 1994; Casper & Jackson, 1997; Robinson & van Vuuren, 1998; Schenk et al., 1999). This review focuses on what these responses actually contribute to the nutrient status of the plant in the context of competition with both other plants and soil microorganisms. The attributes of the patch itself are also considered.

Heterogeneity in resource distribution arises as a result of organic inputs and their subsequent microbial decomposition. These inputs vary widely in their chemical and physical quality, as widely as the material from which they are derived (e.g. leaf litter, dead roots, animal corpses and dead microorganisms). Microbial decomposition of both simple and complex organic materials will release inorganic nutrients for plant capture. However, the spatial and temporal release of these inorganic nutrients will be more complex than simply applying a patch of inorganic nutrients directly. The diffusion of these released inorganic ions in soil also varies. Nitrate (NO3-) is universally soluble in water and has a diffusion coefficient (D) ofapprox. 10-10 m2 s-1 which is close to the diffusion coefficient in free solution. By contrast, phosphate ions absorb strongly to surfaces dominated by A13+, Fe3+ and Ca2+, forming insoluble

complexes, thus the mobility of phosphate ions is much more restricted at approx. 10-13-10-15 m2 s-1 (Tinker & Nye, 2000). Collectively, these processes of organic material input and their subsequent decomposition contribute to the heterogeneous or 'patchy' distribution of nutrient resources in soil.

This variation in nutrient distribution can be considerable. For example, geostatistical analysis has demonstrated that within the rooting zone of an individual plant there can be as much variation in nutrient availability as within an entire 120 m2 plot (Jackson & Caldwell, 1993a, 1993b). Similarly, Farley & Fitter (1999a) found nitrate (NO3-) and ammonium (NH4+) concentrations in the soil solution from a deciduous woodland varied two- to fivefold at scales of only 20 cm and, although there was a degree of seasonality in nutrient variation, the overall temporal pattern was largely unpredictable.

II. Morphological responses When roots encounter a nutrient-rich patch they often proliferate roots within it. But what does root proliferation actually mean? It has been used to cover a range of morphological responses by roots to nutrient patches, including increases in elongation of individual roots Jackson & Caldwell, 1989; Bilbrough & Caldwell, 1995; Zhang & Forde, 1998; Zhang et a., 1999); total root length (van Vuuren et a., 1996; Hodge etal., 1999a, 2000c); root production (Gross et al. 1993; Pregitzer etal., 1993; Hodge et al., 1999b, 2000d); and extent of lateral branching (Larigauderie & Richards, 1994; Farley & Fitter, 1999b). With such a wide definition it is not surprising that proliferation responses are commonly reported.

However, root proliferation strictly involves the initiation of new laterals rather than their elongation; although both can increase root length, lateral initiation is more likely to do so locally. Quantifying lateral initiation is more easily done in some species than in others, which is why total root length in the patch is commonly measured to indicate the total absorptive area in the patch zone. Although less often reported, some roots show no proliferation response to nutrient-rich patches, even when a response may be expected. Poapratensis produced greater root lengths in a control patch containing just the background growth medium than in an organic patch (Hodge et al., 1998), but in another study, when it was in competition with another grass species for the same type of patch, it did proliferate by an increase in root length (Hodge et al., 1999a). Moreover, proliferation responses are far from uniform across species (Campbell et al., 1991; Farley & Fitter, 1999b); even within species the response may be context-dependent. But can any generalizations be made to the extent to which allocation of roots to nutrient-rich zones occurs? First I will consider root biomass allocation.

1. Biomass allocation within the root system

It is often assumed that fast-growing species from fertile habitats show more morphological plasticity to nutrient patches than slow-growing species from infertile habitats, as the higher resource availability in fertile sites offsets the expense of new organ construction (Grime, 1979; Chapin, 1980; Grime et al, 1986; Grime et a., 1991; but see Reynolds & D'Antonio, 1996). Robinson & van Vuuren's (1998) survey on plants grown with a heterogeneous nutrient supply of N, P and/or K found some support for this hypothesis: fast-growing species had a larger 'root size' (root number, length or dry mass) in the nutrient-rich zone than slow-growing species when compared with a uniformly deficient control. This type of control assesses the plant's ability to capture nutrients supplied as a local discrete zone against an otherwise nutrient- poor background, and thus is more relevant to seminatural unfertilized habitats. However, fast-growing species are usually associated with higher background fertility, yet no significant differences occurred between fast- or slow-growing species in comparison to the uniformly high nutrient control. In addition, life form was as important a factor as maximum relative growth rate (RGRma), with forbs proliferating more than grasses. Thus there was only weak support for the general assumption that fast-growing species exhibit greater morphological plasticity. This may be caused by the grouping of root length, mass and number into the general term 'root size' used by Robinson & van Vuuren (1998). What if only root biomass allocation within the root system was considered?

Campbell et al. (1991) studied the root response of competitively dominant and subordinate plant species. Plants were grown in microcosm units onto the surface of which

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nutrients were continuously dripped in four quadrants. By obtaining the correct drip rate, Campbell etal. (1991) were able to present the plant with nutrient-rich or nutrient-poor patches without the use of barriers, thus allowing free root

growth within the unit. The competitively dominant plants had the greatest absolute amount of root in the nutrient-rich zone (and also in the nutrient-poor zone). However, the com-

petitively inferior or subordinate plants located more of their new root growth into the nutrient-rich zone (i.e. they located their roots with more precision). Campbell et al. (1991) referred to this as a contrast between scale and precision of the

response. Although the results of some studies support the

findings of Campbell et al. (1991): (Grime, 1994; Robinson & van Vuuren, 1998; Wijesinghe et al., 2001), others do not

(Einsmann et al., 1999; Farley & Fitter, 1999b; Bliss etal., 2002) and have even reported a tendency for foraging precision to be greater in species with larger root systems (Einsmann et al., 1999; Farley & Fitter, 1999b). These con-

trasting findings may be caused by differences among the various studies in measuring scale and precision. In addition,

Wijesinghe et al. (2001) have recently demonstrated that

precision of foraging is not a fixed property, but varies within

species among different treatments. Thus the environmental context in which the response by the root system is expressed is as important as the response itself.

2. Root diameter and specific root length

Root biomass measurements are not necessarily indicative of the total absorptive area of the root system, and alterations of the root system architecture can occur without a change in the total root biomass. This led Eissenstat & Caldwell (1988) to

suggest that the ability to proliferate roots in patches may be related to specific root length (SRL). SRL, or root length per unit mass (cm mg-1), varies with root diameter and is often

Control (HHH) Phosphate (LHL) NitratE

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used as a surrogate for diameter, but is also influenced by tissue density. Eissenstat (1991) found sweet orange (Citrus

sinensis) rootstocks with the highest SRL had a more rapid rate of root proliferation than those of smaller SRL. The variation in SRL was not entirely explained by differences in root diameter, however, as differences in tissue density also occurred.

Measuring root diameter directly, Fitter (1994) found a close

relationship between the ratio of relative extension rates in a nutrient-rich patch to that in a nutrient-poor patch and the mean root diameter of terminal roots among four related

species in the family Caryophyllaceae (Silene vulgaris, Silene

noctiflora, Silene alba and Agrostemma githago). As expected, the more coarse-rooted (larger diameter) species were much less responsive to the nutrient-rich zone. However, in another

study proliferation of grass roots in an organic patch was not as predicted by SRL (Hodge et al., 1998). In addition to the SRL of the species, the SRL of the roots experiencing the

patch can also alter, and if it does, generally an increase is observed caused by a greater length of thinner roots (Robinson & Rorison, 1983; Fitter, 1985; Farley & Fitter, 1999b).

3. The importance of root proliferation

Drew and coworkers in the 1970s conducted a series of classic

experiments on the response of barley (Hordeum vulgare) plants with only part of their root system exposed to high concentrations of phosphate, ammonium (NH4+), nitrate (NO3-) or potassium (K). Roots responded by increasing the

length and number of primary laterals and secondary laterals to phosphate, NH4+ and NO3- but not K (Drew, 1975; Drew etal., 1973; Drew & Saker, 1975, 1978; Fig. 1). The figures produced by Drew demonstrated that root proliferation can be quite spectacular when it does occur. Intuitively it must therefore be important for enhanced nutrient capture, but does the experimental evidence support this view?

e(LHL) Ammonium (LHL) Potassium (LHL)

Fig. 1 Proliferation of primary and secondary laterals by barley (Hordeum vulgare) grown in solution culture with the middle root section exposed to a 100-fold greater concentration of phosphate, nitrate, ammonium or potassium ions compared with roots above or below (LHL). Controls were supplied with high concentration of nutrients in all zones (HHH). Abbreviations: H, high; L, low, referring to nutrient concentrations experienced by the top, middle and bottom sections of the root system. From Drew (1975) with kind permission from the trustees of the New Phytologist.


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Both as predicted by theoretical models (Baldwin, 1975; Barber & Cushman, 1981; Silberbush & Barber, 1983) and demonstrated experimentally (Fitter et al., 2002), an increase in root-length density is more important for enhanced capture of immobile than mobile ions. Hence the 'benefit' of root proliferation in phosphate-rich patches is relatively easy to interpret. But what about N-rich patches? Barley roots in Drew's (1975) experiment proliferated as much to inorganic N sources as to phosphate, thus it was similarly expected that this proliferation would be beneficial to N capture. Demon-

strating that this was the case, however, proved more troublesome. Three different studies, one on wheat (van Vuuren et al., 1996), the other two using a range of different grass species (Fransen etal., 1998; Hodge et al., 1998), failed to dem- onstrate a relationship between root proliferation in, and N capture from, N-rich organic patches. Hodge et al. (1998) and van Vuuren et al. (1996) used Lolium perenne shoot material as patches, while Fransen etal. (1998) used soil

patches against a sand background. In the study by Hodge et al. (1998) the L. perenne patch material was dual-labelled with 15N and 13C. As only 15N and not 13C enrichment of the

plant material grown with these patches occurred, the plants must have been taking up N from the patch in inorganic form after microbial decomposition. As NO3- is highly mobile in soil it should not be necessary for roots to proliferate as much to this ion as to immobile ions such as phosphate, but this is what they do (Fig. 1). Moreover, molecular evidence con- firmed a direct role for NO3- supplied locally in lateral root elongation rates in Arabidopsis thaliana (Zhang & Forde, 1998; Zhang et al., 1999). The problem of why roots respond to NO3-, however, remained unresolved, or as Robinson (1996) asked, 'why do plants bother?'.

Plants have evolved as members of a community in which both above- and below-ground competitive interactions are of importance in determining resource capture. Surprisingly, below-ground competitive interactions have seldom been studied directly, and most of the literature is based on individual plants or monocultures with competitive interactions inferred from these data. Maina et al. (2002) recently demonstrated that when two bean (Phaseolus varigaris) plants were grown with their root systems split evenly between two pots, overproduction of roots occurred, shoot: root ratios decreased, and reproductive yields declined compared with bean plants grown individually in a single pot. Soybean (Glycine max) plants responded similarly (Gersani et al., 2001). The identity of neighbours can have a large impact on root morphological responses (Huber-Sannwald et al., 1997) and competitive success in patch exploitation (Huber-Sannwald et al., 1996). In the studies by Maina et al. (2002) and Gersani etal. (2001), however, not only the same species but identical vari- eties were grown together. Thus it is puzzling how the roots could distinguish between roots produced by the same plant and those produced by the other in order to result in the observed overproduction of roots.

800 -

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E 0

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600 -

400 -

200 -

U Eo

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20 40 60 80

Root length density (cm cm-3)

100 100

Fig. 2 Nitrogen capture by Lolium perenne (squares) and Poa pratensis (circles) from a patch of decomposing L. perenne shoot material is a simple function of root length density in the patch when the plants are grown in competition. Points shown are means (n = 4) ? SE of plants harvested with time. From Hodge et al. (1999a) with kind permission from Blackwell Science Ltd.

In experiments where two different plant species were grown together for a common organic patch, root proliferation did confer an advantage: there was a direct relationship between root proliferation in, and N capture from, the organic material (Fig. 2; Hodge et al., 1999a; Robinson et al., 1999). As in the study by Hodge et al. (1998), only 15N enrichments and not 13C were detected in the plant tissue, suggesting that N from the organic material was captured in inorganic N form. The organic material added (L. perenne shoots) would have contained a mixture of N sources. Release of N therefore would have occurred both spatially and temporally through- out the patch until microbial decomposition was complete. Thus root proliferation is important for N capture when

plants are in interspecific competition for organic patches containing a finite local supply of mixed N sources. Remove one of these factors and the importance for N capture is obscured. This explains why, when plants are grown as individuals or in monoculture (Wiesler & Horst, 1994; van Vuuren et al., 1996; Hodge et al., 2000c) or in competition for simple inorganic N forms such as NO3- (Fitter et al, 2002), no relationship between root proliferation and N capture could be demonstrated. These results suggest that, in agricul- tural situations, root proliferation may benefit plant N capture only when in mixed cropping systems and when N additions are in slow-release forms. Although Maina et a. (2002) concluded from their work that bean plants with a reduced ability to proliferate roots should be selected for cul- tivation purposes to enhance yields, their variety of bean is

commonly mix-cropped with maize. If the maize proliferates more than the cultivars of bean selected, bean yields may decline further.

Whether a plant proliferates roots in a nutrient patch probably depends on the plant's demand for the nutrient, the mobility of the nutrient within the plant and the strength of

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Table 1 Root proliferation responses in organic patches of Lolium perenne shoots of contrasting C: N ratio, percentage of N originally added in the patch captured by the plant and N captured from the patch as a percentage of total plant N at harvest

Root % N originally N captured from C: N Time proliferation added in patch patch as a % ratio (d) Plant species in patch? captured by plant of total plant N Calculated from

31: 1 39 Festuca arundinacea Yes 4 7 Hodge et al. (1998) 39 Phleum pratense Yes 4 16 39 Poa pratensis No 3 13 39 Dactylis glomerata (Yes) 5 11 39 Lolium perenne Yes 5 10

31: 1 56 Poapratensis* Yes 5 18 Hodge et al. (1999a) 56 L. perenne* Yes 9 16

22: 1 22 Plantago lanceolata and L. perenne* Yes 8 2 Hodge (2003b) 12:1 70 Poa pratensis and L. perenne* No 26 1 Hodge et al. (2000c)

(Yes), proliferation response did occur compared with controls without a patch, but only at final sampling date. *Studies that involved growing plant species together in interspecific competition.

the patch relative to background fertility (Table 1). Prolifera- tion responses to K are perhaps less commonly reported because plants are better able to redistribute K internally to satisfy demand (de Jager, 1982; Scott & Robson, 1991). In the case of N, the data in Table 1 suggest that when patches supply > 10% of the total plant N content, root proliferation occurs. There are exceptions. Poa pratensis did not proliferate roots in an N-rich patch, even when the N captured from the

patch represented 13% of its total N content, but in another

study where patch N represented a larger proportion of its total N (18%), proliferation did occur. By contrast, both L. perenne and Plantago lanceolata proliferated roots when the N captured from the patch represented only 2% of their total N content (Table 1). Different species may have different thresholds for different nutrients before proliferation occurs, and where values representative of natural soils and patches occur on this scale is currently unknown. There also is a need for more studies to measure the benefit of the proliferation response in terms of nutrient capture rather than simply the size of the proliferation response.

4. Broader implications

The limited evidence from studies at the plant population level suggests that, even when individuals within the population respond to, and were affected by, nutrient heterogeneity (Casper & Cahill, 1996), there was a negligible impact at the population level (Casper & Cahill, 1996, 1998; Morris, 1996). However, these studies used plant monocultures and nutrient capture was not followed directly. Nutrient heterogeneity may have a more subtle impact on plant communities. For example, although capture of N from added organic material was similar regardless of whether L. perenne or P pratensiswas grown in monoculture or interspecific competition, within the interspecific treatment P. pratensis (which in this study also produced the greater root lengths) captured more of the N

than L. perenne. Moreover, N capture from the added organic material was independent of the scale of heterogeneity, suggesting that roots were sufficiently plastic in their response to track the scale of heterogeneity and maintain performance (Hodge etal., 2000c). Nutrient supply also varies hetero- geneously down the soil profile and plants differ in their ability to acquire nutrient from different depths (Berendse, 1982, 1983; Veresoglou & Fitter, 1984; Genney et al., 2002). This ability to acquire nutrients at depth can vary depending on which species are present and therefore competing for resources (Berendse, 1981, 1982; D'Antonio & Mahall, 1991; Jumpponen et al., 2002). For example, when in monoculture Achillea millefolium acquired more N (as 15NH4Cl) when injected at 5 cm rather than 20 cm depth. When grown with Festuca ovina, however, Achillea increased its acquisition of N added at the lower injection depth (Jumpponen et al., 2002). In addition, Fitter (1982) demonstrated that heterogeneous arrangement of acidic and calcareous soil resulted in higher plant diversity than a homogenous mixture of the two soils. Collectively, the differences in nutrient-acquisition patterns and the response of different plant species to patches suggests that nutrient heterogeneity promotes species coexistence. However, in addition to differences between species, considerable variation within species can occur depending on the scale of heterogeneity (Wijesinghe et al., 2001).

Plants may also avoid resource competition by displaying root system plasticity. Pea (Pisum sativum) plants with their root system split evenly between two pots (called 'fence- sitters'; Gersani etal., 1998) hardly altered their total root biomass and fitness (measured as fruit d. wt) in response to an increasing number of competing pea plants grown in one of the pots, but the allocation of the fence-sitters' roots between the two pots changed dramatically. For every additional competitor plant added, the fence-sitter shifted 0.12 g of its biomass from the pot containing the competitor plants into the pot with no competitors, so avoiding any detrimental effects

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of competition (Gersani et al., 1998). In the field, such diver- sion of resources into patches free of other competitor roots may not always be possible. Under natural conditions, nutrient concentrations are generally higher in the uppermost layers of the soil profile caused by litter inputs and their subsequent decomposition. Roots are also generally more concentrated in the top layers of the soil profile (McGonigle & Fitter, 1988; Mamolos et al., 1995; Jackson et al., 1996; Leuschner et a., 2001). Because of the natural development of the root system such distributions are to be expected, but in some cases root distributions do not relate to nutrient distributions (Caldwell et al., 1996). Additional constraints on root development and distribution in the field include soil physical and chemical properties, microorganisms both beneficial and detrimental to root growth, interactions with other roots and, at larger scales, the terrestrial biome in which the plant is growing (Jackson etal., 1996; Schenk et al., 1999; Robinson etal., 2003).

III. Root demography Root biomass measurements are often insufficient to determine successful patch exploitation, and give no information about the processes of root production and death that occurred before measurement (Hendrick & Pregitzer, 1992). To follow these processes requires an understanding of root demography. For example, although there was little net change in numbers of Ambrosia artemisiifolia roots in either fertile or H20 control patches, both root birth and death rates increased in the fertile patch, thus root turnover was higher (Gross etal., 1993). Had only root numbers, length or biomass been measured, no response would have been detected. These fine roots associated with patch exploitation are expensive to construct particularly in terms of N, a key resource (Pregitzer etal., 1997). Fransen & de Kroon (2001) studied whether the proliferation of roots in nutrient-rich zones was disadvantageous in the long term by comparing shoot biomass of Holcus lanatus (characteristic of nutrient-rich habitats) and Nardus stricta (characteristic of nutrient-poor habitats) grown over two growing seasons in a heterogeneous nutrient treatment where 50% of the area was nutrient-rich and the other 50% nutrient-poor compared with homogeneous nutrient-rich or nutrient-poor treatments. Holcus proliferated roots of short lifespan preferentially in the nutrient-rich side of the heterogeneous treatment whereas Nardus did not. Nardus roots tended to live longer than Holcus, but this difference was only weakly significant (P = 0.072). Initially Holcus produced more shoot biomass in the heterogeneous treatment, but by the end of the first growing season this advantage had disappeared, and by the end of experiment Holcus biomass in the heterogeneous treatment was similar to that produced in the homogeneous nutrient-poor treatment. By contrast, shoot biomass of Nardus in the heterogeneous treatment was similar to that expected based on shoot biomass production from the homogeneous nutrient arrangements

over both growing seasons. Thus Fransen & de Kroon (2001) concluded that selective placement of short-lived roots in nutrient-rich zones was a disadvantage in the long term. However, these two species tend to grow in different habitats and their different strategies to nutrient patches may be optimal for their particular environment.

Root demography is influenced by a wide range of abiotic and biotic factors including differences among species (Eis- senstat & Yanai, 1997); root order and diameter (Eissenstat etal., 2000; Wells & Eissenstat, 2001); mean radiation flux (Fitter et al., 1998, 1999); temperature (Forbes et al., 1997; Edwards etal., 2004); pathogen populations (Kosola et al., 1995); mycorrhizal colonization (Hooker et al., 1995; Majdi & Nylund, 1996; Hodge, 2001, 2003a; King et al., 2002); and nutrient and water availability (Eissenstat & Yanai, 1997; King et al., 2002). Yet it is still unclear how root death is controlled. The link between plasticity in root branch structure and function (resource acquistion) is also unclear (Pregitzer, 2002). Following demography in trees is particularly difficult because of their widespread root system, and often it is unclear exactly where on the root system the roots being measured occur in relation to other root orders. Although fine root turnover in trees has been extensively studied, there is increasing evidence that all fine roots are not equal among different species, and to classify differences among species simply based on size attributes is unacceptable (Pregitzer et a., 1998, 2002; Pregitzer, 2002).

Therefore it is hardly surprising that no one strategy appears optimal for successful patch exploitation, with increased (Pregitzer et al., 1993), decreased (Hodge et a., 1999c), or no effect (Hodge etal., 2000d) on root longevity in fertile patches being reported. Although some of these differences may be caused by the different plant species studied, a single plant species (L. perenne) displayed a range of demographic responses to L-lysine patches of varying concentration and size, whereas N capture from the L-lysine was a simple function of the amount of N added (Hodge et al., 1999b). Thus the attributes of the patch itself may also influence the longevity of the roots exploiting it.

IV. Physiological plasticity In addition to root morphological responses, physiological alterations in uptake capacity can play an important role in nutrient acquisition. Increased uptake may be caused by a higher uptake capacity (Vm) or a higher ion affinity (low Km) of the roots or, more simply, an increase in nutrient (substrate) concentrations in the nutrient-rich patch. It is often assumed, based largely on the predictions of Grime (1979), that slow- growing species exhibit greater physiological plasticity than fast-growing species, as physiological plasticity is generally viewed as a less expensive alternative for the plant. Robinson & van Vuuren (1998) in their survey of the literature found support for Grime's predictions, but qualified their support by

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emphasizing it is equally important to resolve what these morphological or physiological responses actually achieve in terms of nutrient capture for different species. In other words, the plant response must be measured in the context in which the response is expressed.

When roots of nutrient-deprived plants are supplied with nutrients locally, uptake per unit of root usually increases (in 75% of the cases reviewed by Robinson, 1994). This increase is generally two- to threefold at the maximum (Robinson, 1994), although even greater increases have been reported (fivefold, Drew & Saker, 1978; sevenfold, van Vuuren etaL, 1996, 11-fold, Robinson et aL, 1994). However, such increases are transient (Burns, 1991; Robinson, 1994; van Vuuren et al., 1996). Physiological responses usually occur before morphological ones (Drew & Saker, 1978; Burns, 1991; Caldwell, 1994; van Vuuren et al, 1996), thus increased ion uptake may act as a signal of locally improved soil nutrient status and a trigger for new root investment in the patch zone. It also implies that while root physiological changes may be important in the short term, morphological responses are required for the longer-term exploitation of patches. By contrast, Fransen et al. (2001) concluded from their 2 yr study on competition between Festuca rubra and Anthoxanthum odoratum for nutrients supplied either homogenously or at two levels of heterogeneity, that higher physiological, rather than morphological, plasticity was critical for long-term competitive advantage because in the heterogeneous treatment both E rubra and A. odoratum contained equivalent amounts of strontium (an analogue for Ca and a measure of root activity) injected at the end of the experiment, despite A. odoratum having a sparser root system. So, why do morphological responses occur at all if, as hypothesized by Grime (1979), they are so costly that only plants from fertile sites can 'afford' root proliferation, and if plants maximize nutrient acquisition at minimal cost (Bloom et al., 1985). Could it be the type of resource which is limiting that determines the response?

Physiological plasticity is generally assumed to be more important in enhancing capture of mobile ions, such as NO3-, as uptake is limited not by diffusion in the soil but by uptake at the root surface. By contrast, immobile ions such as phosphate are limited more by diffusion to the root surface, so enhancing ion uptake at the root surface will not greatly enhance phosphate capture. The plant may need to respond rapidly to increase capture of mobile ions before they diffuse to other roots, while a rapid response is less crucial for immobile ions, allowing time for new root construction. Therefore it may be tempting to speculate that physiological responses occur in response to NO3- while morphological responses are more important in enhancing phosphate capture. However, physiological responses may also enhance phosphate capture provided the phosphate patch is exceptionally fertile (Caldwell etal., 1992), and morphological rather than physiological responses were found to be more important for plant N capture in the study by Hodge et al. (1999a). Furthermore,

maintenance of high ion-uptake rates is very energy-consuming (van der Werf et al., 1988), thus they are not necessarily a less expensive alternative to new root growth, particularly in young plants on which most of the literature is based. Simi- larly, Robinson (2001) estimated that root proliferation costs may be as little as 0.2% of the plant's daily carbon gain, although this cost will differ according to the conditions the plant experiences, such as photosynthetic supply, rooting volume and patch size. Burns (1991) suggested that if the cost of maintaining high absorption rates in the part of the root system experiencing the patch becomes too high, the plant may switch to new root production instead. This could explain why alterations in kinetic rates are often reported to occur before root proliferation (Drew & Saker, 1978; van Vuuren et al., 1996) but not why slow-growing species generally exhibit greater physiological plasticity than fast-growing species, unless the balance of cost is seldom in favour of new root growth or the nutrient inputs are so transient their duration is insufficient to trigger new root production.

Caldwell and coworkers, from their field investigations on cold desert species of the Great Basin, USA, have demonstrated that physiological responses of roots extracted from N- P-K solution patches can be both rapid, occurring within a 3 d period, and large, showing as much as 80 and 88% higher uptake rates for phosphate and N, respectively, than control roots extracted from the same plant but which had received an H20 patch (Jackson et al., 1990; Jackson & Caldwell, 1991). Although these values are certainly impressive, their ecological significance may be questionable as they were obtained under laboratory assay conditions. Under natural conditions the ions must diffuse to the root surface at sufficient rates to satisfy this increase in uptake capacity. Expansion of the microbial population in these nutrient patches may effectively block ion diffusion to the root, or block it sufficiently so that the increased uptake rate is ineffectual. However, as the greatest relative increases in NH4+ uptake occurred at the lowest assay concentration (50 pM), which reflected the typical soil solution concentration (Jackson & Caldwell, 1991), this would suggest that such increased uptake kinetics could represent an important mechanism for enhanced nutrient uptake under field conditions. Increased root-uptake kinetics for both NH4+ and NO3- in these cold desert species have also been reported following pulses of simulated rain (BassiriRad & Caldwell, 1992a, 1992b; Cui & Caldwell, 1997a; Ivans et al., 2003), but not always (BassiriRad etal., 1999), and there is considerable variation among these species in their ability to alter uptake kinetics (BassiriRad & Caldwell, 1992a, 1992b; Ivans etal., 2003). A physiological response to these small summer rain events makes more economic sense than produc- ing new roots because of the transient nature of the N pulse, but even this response may play only a minor role. More important were the increases in N diffusion to the root surface because of the elevated soil moisture and the increased microbial turnover of soil N pools releasing N for root capture




New 16 Review Tansley review Phytologist

(Ivans et al., 2003). To understand root responses to nutrient

patches (or pulses) therefore requires an understanding of the interaction between soil microorganisms and the attributes of the nutrient patch itself.

V. Root plasticity in patches in competition and symbiosis with microorganisms Root proliferation, which involves the production of new roots, is generally slow to occur (approx. 35 d for a range of

grasses, Hodge etal., 1998, 1999a), thus it is unlikely that root proliferation allows the plant to compete directly with the microbial community. Experimental evidence also suggests that plant nutrient capture from added organic material starts to increase when microbial and soil fauna populations decline (Griffiths etaL, 1994; Hodge etaL, 2000e). Plants outcompete microorganisms in the long term, probably because of their

longer turnover times (reviewed by Kaye & Hart, 1997;

Hodge et al., 2000a).

Although often ignored in root-proliferation studies, most plant species have an additional mechanism to enhance nutrient acquisition, namely mycorrhizal symbiosis. It is well established that fungi in the ericoid and ectomycorrhizal association possess saprophytic capabilities which enable nutrient

(predominantly N) capture from complex organic sources to which the plant would not normally have direct access (Smith & Read, 1997; Chalot & Brun, 1998). It is also recognized that different fungal species, and even strains of the same

species, differ widely in their ability to capture nutrients from such complex sources (Smith & Read, 1997).

In common with the response of roots, both free-living (Dowson et al., 1989; Ritz et al., 1996) and mycorrhizal sym- biont fungi of both the ectomycorrhizal (Bending & Read, 1995) and AM symbiosis (Mosse, 1959; Nicolson, 1959; St John et al, 1983a, 1983b; Hodge etal., 2001) can proliferate hyphae in nutrient-rich zones, often at the expense of growth

elsewhere. For the purpose of this review, only the response of the colonized root to nutrient patches is of interest, and information from the ectomycorrhizal and ericoid associations is lacking in this respect. A limited amount of data on the

impact of AM colonization is available. As fungal hyphae also

proliferate in patches, and as root proliferation responses are

generally slow to occur, Tibbett (2000) suggested that root

proliferation will become obsolete when roots are colonized

by mycorrhizal fungi. Because of their smaller size, AM

hyphae should: (i) be less expensive to construct than fine roots in terms of C (Fitter, 1991) and presumably N (Pregitzer et al., 1997); (ii) be able to detect and respond to short-lived nutrient patches or pulses that the roots cannot detect; and (iii) be able to penetrate to the sites of patch decomposition and therefore be able to compete directly with other soil

microorganisms for the nutrients released. Also, as AM fungi (AMF) obtain a C supply from their host plant, this should give the AMF a competitive advantage over other soil microorganisms should C become limiting in the patch zone. Thus proliferation of AMF hyphae instead of roots should, in theory, be more beneficial to the host plant, but does the experimental evidence support this view?

The evidence available shows that, generally, AMF have little impact on nutrient capture from patches other than that of P, although there is one report of enhanced N capture, but

only when plants were grown in interspecific competition (Hodge, 2003b; Table 2a). Furthermore, root responses are

demonstrably more important than those of AMF when both are present in the nutrient patch. Three different AMF (Glomus mosseae, Glomus hoi or Scutellospora dipurpurescens) showed different levels of internal colonization and production of external mycelium but, whereas none of the fungal parameters responded to a glycine patch, the roots did. In all cases, including the uncolonized control, net numbers of roots were higher in glycine compared with H20 control

patches (Hodge, 2001). Although in the presence of roots

Table 2 Influence of arbuscular mycorrhizal (AM) colonization on nutrient capture when (a) both roots and AM hyphae are present in the patch, and (b) only AM hyphae have access to the patch

(a) Roots and AM hyphae together in patch Patch added Influence of AM colonization on nutrient capture compared with control* Reference

Glycinet No difference in N capture Hodge (2001) Lolium perenne shootst No difference in N capture Hodge et al. (2000b) NO3-, H2PO-4 No difference in N capture; enhanced P capture Cui & Caldwell (1996a) Soilt Only one species (of seven) showed enhanced P uptake Farley & Fitter (1999b) L. perenne shootst Increased N capture but only when in interspecific plant competition Hodge (2003b)

(b) AM hyphae only in patch Patch added Influence of AM hyphae on nutrient capture compared with control* Reference

NO3-, H2PO4 No difference in N capture; only AM colonized plants captured P Cui & Caldwell (1996b) L. perenne shoots? Enhanced N capture Hodge et al. (2001)

*Controls: studies marked t used an indigenous mycorrhizal control, those marked t used a nonmycorrhizal control; ?Hodge et al. (2001) used an AM-colonized control with hyphae denied access to the patch. Data are from microcosm studies.





AMF may be relatively unresponsive to nutrient patches, they may exert their influence through modifications of the root's

response. AMF colonization has been shown to increase root

production and alter root length densities in patches (Cui & Caldwell, 1996a; Hodge etal., 2000b). Moreover, in the absence of roots AMF have been demonstrated to capture and transfer both P and N (although not when added as NO-) from patches to their host plant (Table 2b). In the field, plants can be linked into a common mycelial network. This has led to the suggestion that plants linked by this common mycelial network may benefit by the redistribution of nutrients along the network, thus reducing the consequences of heterogeneity for individual plants (Ozinga et al., 1997). However, the little

experimental evidence available suggests nutrient transfer

along the common mycelial network occurs only over very short distances (Chiariello et al., 1982; Newman, 1988), and we are only just beginning to address how mycorrhizal fungi may influence, either directly or indirectly, nutrient capture from heterogeneous nutrient supplies.

VI. Influence of patch attributes

Nutrient patches are both spatially and temporally variable. Fitter (1994) further categorized these patches based on various attributes (Fig. 3). The intensity or strength of the

patch encountered is also important. For example, although not measuring root proliferation directly, Jingguo & Bakken (1997) found more root biomass was allocated to N-rich clover patches than to N-poor straw patches, while Jackson & Caldwell (1989) observed that the timing of the response by roots after application of half-strength N-P-K patches was the same as to full strength patches, but the magnitude of the

response was less. The combination of differing responses by plants to patches and intrinsic variation in patches themselves

(Fig. 3) anticipates a wide range of responses in the natural environment. Farley & Fitter (1999b) examined how seven

co-occurring woodland herbaceous perennials responded to

varying patch size (40, 70 or 160 cm3) and quality (100% soil or 50% soil, 50% sand in a background of 100% sand). The

PATCH ATTRIBUTE

DISTRIBUTION

EXTENT

Fig. 3 Basic attributes of patches (distribution, extent and number) on a temporal and spatial scale (after Fitter, 1994) and some predictions of root responses to these patch attributes, all of which will be determined by the strength or intensity of the patch above background fertility.

NUMBER

Root Response

probability of encountering the patch was the same in all treatments. Four (Silene dioica, Veronica montana, Ajuga reptans, Glechoma hederacea) of the seven species proliferated roots by increasing root length in the patch, but only two (S. dioica and V. montana) responded to the quality of the patch, and

only one (G. hederacea) was sensitive to patch size. Such subtle differences in species response to different patches may enable coexistence but, as nutrient capture from the patches was not

directly followed, this cannot be stated with any certainty. The results of the few studies that have investigated some aspect of

patch variation and its impact on plant nutrient capture are shown in Table 3.

Nutrient patches can vary as much on a temporal scale as

they can spatially, yet this aspect has been less well studied (Table 3). The duration of the nutrient pulse had a large impact on N capture by two grass species in the study by Campbell & Grime (1989). By contrast, neither the rate nor the total N captured by another grass species (L. perenne) dif- fered if the patch had been added as a single large addition or as a series of smaller pulses at regular time intervals (Hodge et al., 1999c; Table 3). Similarly, on a spatial scale, varying patch size and concentration had little impact on absolute N and P capture, with only P capture by Artemisia being affected (Cui & Caldwell, 1998; Hodge et al., 1999b; Table 3). Under natural conditions plant root systems will be exposed not to a

single patch but to several, all of which may be of varying nutrient concentration, size and duration. Capture of phosphate by Agropyron and Artemisia from patches added at a 5 cm distance increased as the number of patches increased, even though these patches were of lower nutrient concentration, simply because roots were more likely to encounter them. By contrast, Pseudoroegneria could not detect these

patches and thus hardly captured any phosphate from them (Table 3). Studies on patches of varying durability and

quality, however, have demonstrated that plants can capture large amounts of the N originally available, particularly from simple patches, despite microbial decomposition of the material occurring first (Hodge et al., 2000d, 2000e; Table 3).

SPATIAL

PATTERN

Regular Irregular I I I SIZE I

l I I Large Small

I ABUNDANCE I

i I t Many

I

Morphological

Few I I

TEMPORAL

PREDICTABILITY

I

'

i Predictable Unpredictable

I I I DURATION I

Durable Transient

FREQUENCY I

1 ' 1 Frequent

V

Physiological Morphological

Infrequent

P

Physiological




00

Table 3 Influence of various patch attributes on nutrient capture by different plant species

Scale Patch type

Temporal Nutrient solution

Temporal L-lysine

Spatial L-lysine

Spatial Phosphate

Spatial Nitrate and

phosphate

Spatial Urea

L-lysine Algal amino acids

Algal lyophilized cells L. perenne shoots

Spatial Earthworm L. perenne shoots

Spatial Phosphate

Patch attribute

Nutrient pulses of

varying duration

Small, frequent pulse or a large, single patch*

Differing concentration and volume*

Differing in number, concentration and distance

Two patches of varying quality (both containing NO3- + H2PO4- or one NO3- only and one H2PO4- only)

Organic patches of varying chemical and physical complexity*

Organic patches of

contrasting C: N ratio*

Following addition of a

'primary' patch, additional

patches varying in number and concentration applied

Plant species

Arrhenatherum elatius spp. bulbosum Festuca ovina

Lolium perenne sward

L. perenne sward

Artemisia tridentata

Agropyron desertorum

Pseudoroegneria spicata


Agropyron desertorum

L. perenne sward

L. perenne sward


Nutrient capture from patch

N capture by Arrhenatherum greater from

long-duration pulses and by Festuca from short pulses

No difference in rate or total amount of N captured

Absolute N capture simple function of amount

added; relative N capture depended on

patch concentration

All species captured most P from closest patch. From distant patches, P capture by Artemisia and Agropyron increased with increased

patch number

No difference in N capture. P capture by Artemisia higher from phosphate-only patch

N capture highest from patches of low C: N ratio

N capture highest from lowest C: N ratio (earthworm) patch

Uptake capacity of roots in the primary patch reduced only by highest level of additional patches

Reference

Campbell & Grime (1989)

Hodge et al. (1999c)

Hodge et al. (1999b)

van Auken et al. (1992)

Cui & Caldwell (1998)

Hodge et al. (2000d)

Hodge et al. (2000e)

Duke & Caldwell (2000)

*These studies used 13C, 15N dual-labelled organic material as patches. At no time were 13C enrichments detected in the plant tissue.

b CD

:3- 0

0

?

0

0

N

M' r+ 0n FQ

1N

?rDr

con r-t




Roots are also likely to encounter different patches at different times. When part of the root system locates a new patch, root proliferation in the original patch may be subject to higher turnover if nutrients in the original patch are depleted, and if the new patch contains sufficient nutrient concentrations to divert resources away. Thus, a plant root system should be capable of exploiting a number of patches at the same time, although root proliferation and/or enhanced nutrient uptake of roots in these patches may be expected to be reduced or 'damped down'. By contrast, Duke & Caldwell (2000) found that, although roots exposed to an initial or 'primary patch' containing phosphate had greater uptake capacities than controls receiving no soil phosphate amendment, the addition of further patches to other areas of the root system did not reduce the uptake capacity of roots in the primary patch except at the highest level of additional phosphate amendment (Table 3). Thus there was no clear evidence that root-uptake capacities in the primary patch were regulated by the overall nutrient enrichment of the root system. Also, there was no apparent increase in uptake capacities of roots exposed to the additional patches of low and medium concentrations compared with controls (Duke & Caldwell, 2000). Plant tissue P concentration did not differ among treatments. This may have been because the increased soil phosphate concentrations resulted in P acquisition which met the demands of the plant, even though generally uptake capacities did not alter.

Compared with root responses to patches, the attributes of the patch itself have largely been ignored, with most studies applying a single heterogeneous treatment in comparison to a uniformly nutrient-rich or deficient control. However the dynamics of organic patch decomposition can be as important as the root response to these patches (Hodge et al., 2000d; 2000e). Only by following both together can we understand why different plant species respond to varying patches in certain ways. Moreover, plant capture from nutrient patches, whether in organic or inorganic form, will depend not only on the response of the plant's root system itself, but also on complex interactions with other plant roots, soil microorganisms and fauna, and physical/chemical interactions in the soil (Schenk et al., 1999; Hodge et al., 2000d; Bengough, 2003; de Kroon et al., 2003). If these factors are ignored, the relevance of the plant response to patches may be open to misinterpretation. For example, in the competition study by Hodge et al. (1999a), if the patch had been added as an NO3--rich solution it is questionable whether the 'benefit' of enhanced root length production by L. perennewould have been observed because of the rapid mobility of the NO3- ion in soil. More studies using relevant material, such as dead roots, leaves, soil animals, etc., as patches added to soil systems, and close monitoring of the decomposition dynamics of such material, are required to place root responses and the subsequent decomposition and nutrient capture from patches in a more appropriate ecological context.

VII. Control of root proliferation Both root physiological and morphological plasticity comes at the price of ATP expenditure to maintain high ion-uptake capacities, construction of new roots or increased extension rates of existing roots. Often, reduced growth outside the patch zone is observed (Drew, 1975; Granato & Raper, 1989; Gersani & Sachs, 1992; Linkohr etal., 2002), which may offset some of the cost of new root production inside the patch. Moreover, it seems reasonable to assume these costs must provide a net benefit (and, as discussed above, under certain conditions have been demonstrated to do so); but what happens when photosynthetic supply becomes restricted?

A rather severe (but ecologically realistic) method of reducing photosynthetic supply to the roots is by clipping or grazing; a less invasive method is achieved by shading. Following clipping of 80% of the shoot material of three semiarid range grasses the differences between the species in response to nutrient treatment did not alter but were further exaggerated (Arredondo & Johnson, 1999). Studies comparing shaded and unshaded plants have demonstrated that exploitation of phosphate patches is particularly demanding of photosynthetic C supply (Jackson & Caldwell, 1992; Cui & Caldwell, 1997b). Shading can also reduce the physiological uptake of N (Cui & Caldwell, 1997b), but not always (Jackson & Caldwell, 1992), probably depending on the N demand by the plant at the time. Relative growth rate (RGR) of roots in nutrient-rich patches can also be adversely affected by shading. The RGR ofAgropyron desertorum roots in N-rich patches was reduced by more than 50%, while root RGR in H20 control patches was unaffected (Bilbrough & Caldwell, 1995). Shading may exert its influence through a reduction of the total nonstructural carbohydrate concentration, particularly in shoots (Jackson & Caldwell, 1992).

Shading may also alter root plasticity differently and thus influence competitive interactions. While unshaded sweetgum (Liquidambar styraciflua) was more plastic than loblolly pine (Pinus taeda), when shaded both were equally plastic because of shaded loblolly pine allocating its roots with more precision (Mou et al., 1997). Both Heliocarpus pallidus and Caesalpinia eriostachys monocultures showed enhanced root proliferation in fertile patches when light levels increased, but when grown together in interspecific competition, root proliferation by the fast-growing Heliocarpus was reduced under both high and low light levels whereas Caesalpinia was affected only by low light (Huante et al., 1998). Collectively, these studies indicate that capture of heterogeneous nutrient supplies requires considerable C investment by the plant. If shading simply reduced the nutrient demand by the plant, then capture of nutrients would be lower regardless of their spatial placement. Clearly this is not the case. Moreover, shaded (30% of full sunlight) sweetgum and loblolly pine seedlings had reduced total biomass when grown in a patchy environment than when grown in a uniform nutrient environment





(Mou et aL, 1997), again highlighting that growth in patches is more expensive than under uniform conditions.

The identification of the first component of the NO3- signalling system, the gene ANR1, by Zhang & Forde (1998) represented a major step forward in understanding how root proliferation is controlled. In addition, an Arabidopsis mutant (nial nia2) with very low nitrate reductase activity (0.5% of that found in the wild type) showed a similar response to NO3--rich zones, implying that the signal for increased mer- istematic activity comes from the NO3- ion itself, not a prod- uct of NO3- metabolism (Zhang & Forde, 1998). Subsequent work by Forde and coworkers (Zhang et al., 1999; Zhang & Forde, 2000; Forde, 2002) has suggested that the auxin- sensitive gene axr4may also be involved in the NO3- signal transduction pathway because of the failure of axr4 mutants to respond to localized NO3- additions. By contrast, Linkohr et al. (2002) found that several auxin-resistant mutants including axr4 responded to localized NO3--rich zones in the same manner as the wild type. Although auxin plays an important role in many plant growth, development and physiological processes, including being involved in lateral root development (Evans etal., 1994; Boerjan et al., 1995), the results of Linkohr et al. (2002) argue against a role for auxin in the NO3- signal transduction pathway. Similarly, using phosphate-rich patches, Williamson etal. (2001) reported wild-type Arabidopsis root-system architecture changes in the auxin mutants axrl, auxl and axr4, suggesting that auxin does not play a role in root responses to phosphate-rich patches either. More research into the mechanistic control of root proliferation responses is still clearly required, but with the recent sequencing of the Arabidopsis genome research advances in this area should be forthcoming.

VIII. Conclusions Root morphological and physiological responses are far from uniform across species, and even within species the size of the response depends on the scale of heterogeneity. Future research should focus on the importance of root plasticity for nutrient capture rather than simply measuring the size of the response. This also involves more accurate measurements of the costs associated with physiological and morphological responses andgrowing plants under more ecologically relevant conditions with more realistic patch materials. Moreover, the proliferation by roots observed under controlled conditions, which are generally manipulated so as to maximize such responses, is likely to be significantly reduced under natural conditions where other environmental factors will influence plant growth responses. Most of the data reviewed in this paper come from studies using only one or two plants grown at a time. More studies at the plant community level are required if we are to determine whether heterogeneity is important for plant community dynamics or simply exerts its influence locally on individual members in the community.

Such studies are technically challenging, but are essential and should benefit from the application of molecular approaches. For example, by the use of molecular markers, Jackson and coworkers (Jackson et al., 1999; Linder et a., 2000) were able to trace the distribution of roots in soil. If such approaches could be combined with microbial and nutrient distributions, our understanding of plant competitive interactions in patchy soils would be greatly advanced.

At the other end of the spectrum, molecular research is also needed on the signal pathways involved in root proliferation responses. Some progress has been made with the finding that nitrate is involved directly in at least part of the signal pathway, and the identification of the nitrate-inducible gene ANR1, in root proliferation responses of Arabidopsis, but it remains to be determined whether other ions (notably phosphate) are equally specific. The use of model plants such as Arabidopsis lend themselves to such molecular investigations, but ultimately if more ecologically important issues relating to plant responses to soil heterogeneity are to be addressed then a wider range of plant species from different habitats must be examined.

Acknowledgements A. H. is funded by a BBSRC David Phillips Research Fellow- ship. I thank Alastair Fitter, Richard Norby, Rob Jackson and two anonymous referees for their extremely helpful comments on the manuscript.

References Arredondo JT, Johnson DA. 1999. Root architecture and biomass allocation

of three grasses in response to nonuniform supply of nutrients and shoot defoliation. New Phytologist 143: 373-385.

van Auken OW, Manwaring JH, Caldwell MM. 1992. Effectiveness of phosphate acquisition by juvenile cold-desert perennials from different patterns of fertile-soil microsites. Oecologia 91: 1-6.

Baldwin JP. 1975. A quantitative analysis of the factors affecting plant nutrient uptake from some soils. Journal of Soil Science 26: 195-206.

Barber SA, Cushman JH. 1981. Nutrient uptake model for agronomic crops. In: Iskander IK, ed. Modelling wastewater renovationfor land treatment. New York, NY, USA: Wiley, 382-409.

BassiriRad H, Caldwell MM. 1992a. Temporal changes in root growth and N-15 uptake and water relations of two tussock grass species recovering from water stress. Physiologia Plantarum 86: 525-531.

BassiriRad H, Caldwell MM. 1992b. Root growth, osmotic adjustment and NO3- uptake during and after a period of drought in Artemisia tridentata. Australian Journal of Plant Physiology 19: 493-500.

BassiriRad H, Tremmel DC, Virginia A, Reynolds JF, de Soyna AG. 1999. Short-term patterns in water and nitrogen acquisition by two desert shrubs following a simulated summer rain. Plant Ecology 145: 27-36.

Bending GD, Read DJ. 1995. The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. The foraging behaviour of ectomycorrhizal mycelium and the translocation of nutrients from expo- lited organic matter. New Phytologist 130: 401-409.

Bengough AG. 2003. Root growth and function in relation to soil structure, composition, and strength. In: de Kroon H, Visser EJW, eds. Root ecology. Ecologicalstudies, Vol. 168. Berlin, Germany: Springer-Verlag, 151-171.





Berendse F. 1981. Competition between plants with different rooting depths. II. Pot experiments. Oecologia 48: 334-341.

Berendse F. 1982. Competition between plant populations with different

rooting depths. III. Field experiments. Oecologia 53: 50-55. Berendse F. 1983. Interspecific competition and niche differentiation

between Plantago lanceolata and Anthoxanthum odoratum in a natural hayfield. Journal ofEcology 71: 379-390.

Bilbrough CJ, Caldwell MM. 1995. The effects of shading and N status on root proliferation in nutrient patches by the perennial grass Agropyron desertorum in the field. Oecologia 103: 10-16.

Bliss K, Jones RH, Mitchell RJ, Mou PP. 2002. Are competitive interactions influenced by spatial nutrient heterogeneity and root foraging behavior? New Phytologist 154: 409-417.

Bloom AJ, Chapin FS, Mooney HA. 1985. Resource limitation in plants - an economic analogy. AnnualReview ofEcology andSystematics 16: 363-392.

Boerjan W, Cervera M-T, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Van Onckelen H, Van Monatgu M, Inze D. 1995. Superroot, a recessive mutation in Arabidopsis, confers auxin expression. Plant Cell7: 1405-1419.

Burns IG. 1991. Short- and long-term effects of a change in the spatial distribution of nitrate in the root zone on nitrogen uptake, growth and root development of young lettuce plants. Plant, Cell 6 Environment 14: 21-33.

Caldwell MM. 1994. Exploiting nutrients in fertile soil microsites. In: Caldwell MM, Pearcy RW, eds. Exploitation of environmental heterogeneity ofplants. New York, NY, USA: Academic Press, 325-347.

Caldwell MM, Dudley LM, Lilieholm B. 1992. Soil solution phosphate, root uptake kinetics and nutrient acquisition: implications for a patchy soil environment. Oecologia 89: 305-309.

Caldwell MM, Manwaring JH, Durham SL. 1996. Species interactions at the level of fine roots in the field: influence of soil nutrient heterogeneity and plant size. Oecologia 106: 440-447.

Campbell BD, Grime JP. 1989. A comparative study of plant responsiveness to the duration of episodes of mineral nutrient enrichment. New

Phytologist 112: 261-267.

Campbell BD, GrimeJP, MackeyJML. 1991. A trade-offbetween scale and precision in resource foraging. Oecologia 87: 532-538.

Casper BB, Cahill JF Jr. 1996. Limited effects of soil nutrient heterogeneity on populations of Abutilon theophrasti (Malvaceae). American Journal of Botany85: 333-341.

Casper BB, Cahill Jr JF. 1998. Population level responses to nutrient heterogeneity and density by Abutilon theophrasti (Malvaceae): an experimental neighborhood approach. American Journal of Botany 85: 1680-1687.

Casper BB, Jackson RB. 1997. Plant competition underground. Annual Review ofEcology and Systematics 28: 545-570.

Chalot M, Brun A. 1998. Physiology of organic acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiology Reviews 22: 21-44.

Chapin FS III. 1980. The mineral nutrition of wild plants. Annual Review ofEcological Systematics 11: 233-260.

Chiariello N, Hickman JC, Mooney HA. 1982. Endomycorrhizal role for interspecific transfer of phosphorus in a community of annual plants. Science 217: 941- 943.

Cui M, Caldwell MM. 1996a. Facilitation of plant phosphate acquisition by arbuscular mycorrhizas from enriched soil patches. I. Roots and hyphae exploiting the same soil volume. New Phytologist 133: 453-460.

Cui M, Caldwell MM. 1996b. Facilitation of plant phosphate acquisition by arbuscular mycorrhizas from enriched soil patches. II. Hyphae exploiting root-free soil. New Phytologist 133: 461-467.

Cui M, Caldwell MM. 1997a. A large ephemeral release of nitrogen upon wetting a dry soil and corresponding root responses in the field. Plant and Soil 191: 291-299.

Cui M, Caldwell MM. 1997b. Shading reduces exploitation of soil nitrate and phosphate byAgropyron desertorum and Artemisia tridentata from soils with patchy and uniform nutrient distributions. Oecologia 109: 177-183.

Cui M, Caldwell MM. 1998. Nitrate and phosphate uptake by Agropyron desertorum and Artemisia tridentata from soil patches with balanced and unbalanced nitrate and phosphate supply. New Phytologist 139: 267-272.

D'Antonio CM, Mahall BE. 1991. Root profiles and competition between the invasive, exotic perennial, Carpobrotus edulis, and two native shrub species in California coastal scrub. American Journal ofBotany 78: 885-894.

Dowson CG, Springham P, Rayner ADM, Boddy L. 1989. Resource relationships of foraging mycelial systems of Phanerochaete velutina and Hypholomafasciculare in soil. New Phytologist 111: 501-509.

Drew MC. 1975. Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist 75: 479-490.

Drew MC, Saker LR. 1975. Nutrient supply and the growth of the seminal root system in barley. II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. Journal of Experimental Botany 26: 79-90.

Drew MC, Saker LR. 1978. Nutrient supply and the growth of the seminal root system in barley. III. Compensatory increases in growth of lateral roots, and in rates of phosphate uptake in response to a localised supply of phosphate. Journal of Experimental Botany 29: 435 -451.

Drew MC, Saker LR, Ashley TW. 1973. Nutrient supply and the growth of the seminal root system in barley. I. The effect of nitrate concentration on the growth of axes and laterals. Journal of Experimental Botany 24: 1189-1202.

Duke SE, Caldwell MM. 2000. Phosphate uptake kinetics of Artemisia tridentata roots exposed to multiple soil enriched-nutrient patches. Flora 195: 154-164.

Edwards EJ, Benham DG, Marland LA, Fitter AH. 2004. Root production is determined by radiation flux in a temperate grassland. Global Change Biology (In press.)

Einsmann JC, Jones RH, Mou P, Mitchell RJ. 1999. Nutrient foraging traits in 10 co-occurring plant species of contrasting life forms. Journal of Ecology 87: 609-619.

Eissenstat DM. 1991. On the relationship between specific root length and the rate of root proliferation: a field study using citrus rootstocks. New Phytologist 118: 63-68.

Eissenstat DM, Caldwell MM. 1988. Seasonal timing of root growth in favorable microsites. Ecology 69: 870-873.

Eissenstat DM, Yanai RD. 1997. The ecology of root lifespan. Advances in EcologicalResearch 27: 1-60.

Eissenstat DM, Wells CE, Yanai RD, WhitbeckJL. 2000. Building roots in a changing environment: implications for root longevity. New Phytologist 147: 33-42.

Evans ML, Ishikawa H, Estelle MA. 1994. Responses of Arabidopsis roots to auxin studied with high temporal resolution: comparison ofwild-type and auxin-resistant mutants. Planta 194: 215-222.

Farley RA, Fitter AH. 1999a. Temporal and spatial variation in soil resources in a deciduous woodland. Journal ofEcology 87: 688-696.

Farley RA, FitterAH. 1999b. The response of seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. Journal ofEcology 87: 849-859.

Fitter AH. 1982. Influence of soil heterogeneity on the co-existence of grassland species. Journal ofEcology 70: 139-148.

Fitter AH. 1985. Functional significance of root morphology and root system architecture. In: Fitter AH, Atkinson D, Read DJ, Usher MB, eds. Ecological interactions in soil. Oxford, UK: Blackwell Scientific Publications, 87-106.

Fitter AH. 1991. Costs and benefits of mycorrhizas: implications for functioning under natural conditions. Experientia 47: 350-355.

? New Phytologist(2004) 162: 9-24 www.newphytologist.org




Fitter AH. 1994. Architecture and biomass allocation as components of the

plastic response of root systems to soil heterogeneity. In: Caldwell MM,

Pearcy RW, eds. Exploitation ofenvironmental heterogeneity ofplants. New York, NY, USA: Academic Press, 305-323.

Fitter AH, Graves JD, Self GK, Brown TK, Bogie D, Taylor K. 1998. Root

production, turnover and respiration under two grassland types along an altitudinal gradient: influence of temperature and solar radiation.

Oecologia 114: 20-30. Fitter AH, Self GK, Brown TK, Bogie DS, Graves JD, Benham D,

Ineson P. 1999. Root production and turnover in an upland grassland subjected to artificial soil warming respond to radiation flux and nutrients, not temperature. Oecologia 120: 575-581.

Fitter AH, Williamson L, Linkohr B, Leyser 0. 2002. Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proceedings of the Royal Society of London, Series B 269: 2017-2022.

Forbes PJ, Black KE, Hooker JE. 1997. Temperature-induced alteration to root longevity in Lolium perenne. Plant and Soil 190: 87-90.

Forde BG. 2002. Local and long-range signaling pathways regulating plant responses to nitrate. Annual Review ofPlant Biology 53: 203-224.

Fransen B, de Kroon H. 2001. Long-term disadvantages of selective root

placement: root proliferation and shoot biomass of two perennial grass species in a 2-year experiment. Journal ofEcology 89: 711-722.

Fransen B, de Kroon H, Berendse F. 1998. Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia 115: 351-358.

Fransen B, de Kroon H, Berendse F. 2001. Soil nutrient heterogeneity alters

competition between two perennial grass species. Ecology 82: 2534-2546. Genney DR, Alexander IJ, Hartley SE. 2002. Soil organic matter

distribution and below-ground competition between Calluna vulgaris and Nardus stricta. Functional Ecology 16: 664-670.

Gersani M, Sachs T. 1992. Developmental correlations between roots in

heterogeneous environments. Plant, Cell &i Environment 15: 463-469. Gersani M, Abramsky Z, Falik 0. 1998. Density-dependent habitat

selection in plants. Evolutionary Ecology 12: 223-234. Gersani M, Brown JS, O'Brien EE, Maina GM, Abramsky Z. 2001.

Tragedy of the commons as a result of root competition. Journal ofEcology 89: 660-669.

Granato TC, Raper CD Jr. 1989. Proliferation of maize (Zea mays L.) roots in response to localized supply of nitrate. Journal ofExperimental Botany 40: 263-275.

Griffiths BS, van Vuuren MMI, Robinson D. 1994. Microbial grazer populations in a ]5N labelled organic residue and the uptake of residue N

by wheat. European Journal ofAgronomy 3: 321-325. Grime JP. 1979. Plant strategies and vegtation processes. Chichester, UK:

Wiley. Grime JP. 1994. The role of plasticity in exploiting environmental

heterogeneity. In: Caldwell MM, Pearcy RW, eds. Exploitation of environmentalheterogeneity ofplants. New York, NY, USA: Academic Press, 1-19.

Grime JP, Crick JC, Rincon JE. 1986. The ecological significance of plasticity. In: Jennings DH, Trewavas AJ, eds. Plasticity in plants. Cambridge, UK: Company of Biologists, 5-30.

Grime JP, Campbell BD, Mackey JML, Crick JC. 1991. Root plasticity, nitrogen capture and competitive ability. In: Atkinson D, ed. Plant root growth: an ecologicalperspective. Oxford, UK: Blackwell Scientific Publications, 381-397.

Gross KL, Peters A, Pregitzer KS. 1993. Fine root growth and demographic responses to nutrient patches in four old-field plant species. Oecologia 95: 61-64.

Hendrick RL, Pregitzer KS. 1992. The demography of fine roots in a northern hardwood forest. Ecology 73: 1094-1104.

Hodge A. 2001. Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytologist 151: 725-734.

Hodge A. 2003a. N capture by Plantago lanceolata and Brassica napus from

organic material: the influence of spatial dispersion, plant competition and an arbuscular mycorrhizal fungus. Journal of Experimental Botany 54: 2331-2342.

Hodge A. 2003b. Plant nitrogen capture from organic matter as affected by spatial dispersion, interspecific competition and mycorrhizal colonization. New Phytologist 157: 303-314.

Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 1998. Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. New Phytologist 139: 479-494.

Hodge A, Robinson D, Griffiths BS, Fitter AH. 1999a. Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant, Cell eEnvironment22: 811-820.

Hodge A, Robinson D, Griffiths BS, Fitter AH. 1999b. Nitrogen capture by plants grown in N-rich organic patches of contrasting size and strength. Journal of Experimental Botany 50: 1243-1252.

HodgeA, StewartJ, Robinson D, Griffiths BS, FitterAH. 1999c. Plant, soil fauna and microbial responses to N-rich organic patches of contrasting temporal availability. Soil Biology and Biochemistry 31: 1517-1530.

Hodge A, Robinson D, Fitter AH. 2000a. Are microorganisms more effective than plants at competing for nitrogen? Trends in Plant Science 5: 304-308.

Hodge A, Robinson D, Fitter AH. 2000b. An arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in soil. New Phytologist 145: 575-584.

Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 2000c. Spatial and physical heterogeneity of N supply from soil does not influence N

capture by two grass species. FunctionalEcology 14: 645-653.

Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 2000d.

Competition between roots and soil micro-organisms for nutrients from

nitrogen-rich patches of varying complexity. Journal of Ecology 88: 150-164.

Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 2000e. Plant N

capture and microfaunal dynamics from decomping grass and earthworm residues in soil. Soil Biology and Biochemistry 32: 1763-1772.

Hodge A, Campbell CD, Fitter AH. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from

organic material. Nature 413: 297-299.;j HookerJE, Black KE, Perry RL, Atkinson D. 1995. Arbuscular mycorrhizal

fungi induced alteration to root longevity of poplar. Plant and Soil 172: 327-329.

Huante P, Rinc6n E, Chapin FS III. 1998. Foraging for nutrients, responses to changes in light, and competition in tropical deciduous tree seedlings. Oecologia 117: 209-216.

Huber-Sannwald E, Pyke DA, Caldwell MM. 1996. Morphological plasticity following species-species recognition and competition in two

perennial grasses. American Journal ofBotany 83: 919-931. Huber-Sannwald E, Pyke DA, Caldwell MM. 1997. Perception of

neighbouring plants by rhizomes and roots: morphological manifestations of a clonal plant. Canadian Journal of Botany 75: 2146-2157.

Hutchings MJ, de Kroon H. 1994. Foraging in plants: the role of morphological plasticity in resource acquistion. Advances in Ecological Research 25: 159-238.

Ivans CY, LefflerAJ, Spaulding U, StarkJM, Ryel RJ, Caldwell MM. 2003. Root responses and nitrogen acquisition by Artemisia tridentata and Agropyron desertorum following small summer rainfall events. Oecologia 134: 317-324.

Jackson RB, Caldwell MM. 1989. The timing and degree of root proliferation in fertile-soil microsites for three cold-desert perennials. Oecologia 81: 149-153.

Jackson RB, Caldwell MM. 1991. Kinetic responses of Pseudoroegneria root to localized soil enrichment. Plant and Soil 138: 231-238.

Jackson RB, Caldwell MM. 1992. Shading and the capture of localized soil nutrients: nutrient contents, carbohydrates, and root uptake kinetics of a perennial tussock grass. Oecologia 91: 457-462.





Jackson RB, Caldwell MM. 1993a. Geostatistical patterns of soil

heterogeneity around individual perennial plants. Journal ofEcology 81: 683-692.

Jackson RB, Caldwell MM. 1993b. The scale of nutrient heterogeneity around individual plants and its quantification with geostatistics. Ecology 74: 612-614.

Jackson RB, Manwaring JH, Caldwell MM. 1990. Rapid physiological adjustment of roots to localized soil enrichment. Nature 344: 58-60.

Jackson RB, CanadellJ, EhleringerJR, Mooney HA, Sala OE, Schulze ED. 1996. A global analysis of root distributions for terrestrial biomes. Oecologia 108: 389-411.

Jackson RB, Moore LA, Hoffinann WA, Pockman WT, Linder CR. 1999.

Ecosystem rooting depth determined with caves and DNA. Proceedings of the NationalAcademy of Sciences, USA 96: 11387-11392.

de Jager A. 1982. Effects of localized supply of H2PO4, NO3, S04, Ca and K on the production and distribution of dry matter in young maize plants. Netherlands Journal ofAgricultural Science 30: 193-203.

Jingguo W, Bakken LR. 1997. Competition for nitrogen during decomposition of plant residues in soil: effect of spatial placement of N-rich and N-poor plant residues. Soil Biology and Biochemistry 29:153-162.

Jumpponen A, Hogberg P, Huss-Danell K, Mulder CPH. 2002.

Interspecific and spatial differences in nitrogen uptake in monocultures and two-species mixtures in north European grasslands. FunctionalEcology 16:454-461.

Kaye JP, Hart SC. 1997. Competition for nitrogen between plants and soil

micro-organisms. Trends in Ecology and Evolution 12: 139-143. KingJS, Albaugh TJ, Allen HL, Buford M, Strain BR, Dougherty P. 2002.

Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine. New Phytologist 154: 389-398.

Kosola KR, Eissenstat DM, GrahamJH. 1995. Root demography of mature citrus trees: the influence of Phytophthora nictianae. Plant and Soil 171: 283-288.

de Kroon H, Mommer L, Nishiwaki A. 2003. Root competition: towards a mechanistic understanding. In: de Kroon H, Visser EJW, eds. Root Ecology. Ecological Studies, Vol. 168. Berlin, Germany: Springer-Verlag, 215-234.

Larigauderie A, Richards JH. 1994. Root proliferation characteristics of seven perennial arid-land grasses in nutrient-enriched microsites. Oecologia 99: 102-111.

Leuschner C, Hertel D, Coners H, Biittner V. 2001. Root competition between beech and oak: a hypothesis. Oecologia 126: 276-284.

Linder CR, Moore LA, Jackson RB. 2000. A universal molecular method for identifying underground plant parts to species. Molecular Ecology 9: 1549-1559.

Linkohr BI, Williamson LC, Fitter AH, Leyser HMO. 2002. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. PlantJournal29: 751-760.

Maina GG, Brown JS, Gersani M. 2002. Intra-plant versus inter-plant root competition in beans: avoidance, resource matching or tragedy of the commons. Plant Ecology 160: 235-247.

Majdi H, Nylund J-E. 1996. Does liquid fertilization affect fine root dynamics and lifespan of mycorrhizal short roots? Plant and Soil 185: 305-309.

Mamolos AP, Elisseou GK, Veresoglou DS. 1995. Depth of root activity of coexisting grassland species in relation to N and P additions, measured using nonradioactive tracers. Journal ofEcology 83: 643-652.

McGonigle TP, Fitter AH. 1988. Ecological consequences of arthropod grazing on VA mycorrhizal fungi. Proceedings of the Royal Society of Edinburgh, Series B 94: 25-32.

Morris EC. 1996. Effect of localized placement of nutrients on root competition in self-thinning populations. Annals ofBotany 78: 353-364.

Mosse B. 1959. Observations on the extramatrical mycelium of a vesicular-arbuscular endophyte. Transactions of the British Mycological Society 42: 439-448.

Mou P, Mitchell RJ, Jones RH. 1997. Root distribution of two tree species under a heterogeneous nutrient environment. Journal ofApplied Ecology 34: 645-656.

Newman El. 1988. Mycorrhizal links between plants: their functioning and ecological significance. Advances in Ecological Research 18: 243-270.

Nicolson TH. 1959. Mycorrhiza in the Gramineae. I. Vesicular-arbuscular

endophytes, with special reference to the external phase. Transactions ofthe British Mycological Society 42: 421-438.

Ozinga WA, Van Andel J, McDonnell-Alexander MP. 1997. Nutritional soil heterogeneity and mycorrhiza as determinants of plant species diversity. Acta Botanica Neerlandica 46: 237-254.

Pregitzer KS. 2002. Fine roots of trees - a new perspective. New Phytologist 154: 267-270.

Pregitzer KS, Hendrick RL, Fogel R. 1993. The demography of fine roots in response to patches of water and nitrogen. New Phytologist 125: 575-580.

Pregitzer KS, Kubiske ME, Yu CK, Hendrick RL. 1997. Relationships among root branch order, carbon, and nitrogen in four temperate species. Oecologia 111: 302-308.

Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR. 1998. Variation in sugar maple root respiration with root diameter and soil

depth. Tree Physiology 18: 665-670.

Pregitzer KS, DeForestJL, Burton AJ, Allen MF, Ruess RW, Hendrick RL. 2002. Fine root architecture of nine North American trees. Ecological Monographs 72: 293-309.

Reynolds HL, D'Antonio C. 1996. The ecological significance of plasticity in root weight ratio in response to nitrogen: opinion. Plant and Soil 185: 75-97.

Ritz K, Millar SM, Crawford JW. 1996. Detailed visualization of hyphal distribution in fungal mycelia growing in heterogeneous nutritional environments. Journal of Microbiological Methods 25: 23-28.

Robinson D. 1994. The responses of plants to non-uniform supplies of nutrients. New Phytologist 127: 635-674.

Robinson D. 1996. Resource capture by localized root proliferation: Why do

plants bother? Annals of Botany 77: 179-186. Robinson D. 2001. Root proliferation, nitrate inflow and their carbon costs

during nitrogen capture by competing plants in patchy soil. Plant andSoil 232:41-50.

Robinson D, Rorison IH. 1983. A comparison of the responses of Lolium perenne L. Holcus lanatus L. and Deschampsiaflexuosa (L.) Trin. to a localized supply of nitrogen. New Phytologist94: 263-273.

Robinson D, van Vuuren MMI. 1998. Responses of wild plants to nutrient patches in relation to growth rate and life-form. In: Lambers H, Poorter H, van Vuuren MMI, eds. Variation in plant growth. Leiden, The Netherlands: Backhuys, 237-257.

Robinson D, Linehan DJ, Gordon DC. 1994. Capture of nitrate from soil by wheat in relation to root length, nitrogen inflow and availability. New Phytologist 128: 297-305.

Robinson D, Hodge A, Griffiths BS, Fitter AH. 1999. Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proceedings of the Royal Society ofLondon, Series B 265: 431-435.

Robinson D, Hodge A, Fitter AH. 2003. Constraints on the form and function of root systems. In: de Kroon H, Visser EJW, eds. Root ecology. Ecologicalstudies, Vol. 168. Berlin, Germany: Springer-Verlag, 1-31.

Schenk HJ, Callaway RM, Mahall BE. 1999. Spatial root segregation: are plants territorial? Advances in Ecological Research 28: 145-180.

Scott BJ, Robson AD. 1991. The distribution of Mg, P and K in the split roots of subterranean clover. Annals of Botany 67: 251 -256.

Silberbush M, Barber SA. 1983. Sensitivity of simulated phosphorus uptake to parameters used by a mechanistic-mathematical model. Plant and Soil 36: 461-473.

Smith SE, Read DJ. 1997. Mycorrhizal symbiosis. London, UK: Academic Press.





St John TV, Coleman DC, Reid CPP. 1983a. Association of vesicular-arbuscular mycorrhizal hyphae with soil organic particles. Ecology 64: 957-959.

St John TV, Coleman DC, Reid CPP. 1983b. Growth and spatial distribution of nutrient-absorbing organs: selective exploitation of soil

heterogeneity. Plant and Soil71: 487-493. Tibbett M. 2000. Roots, foraging and the exploitation of soil nutrient

patches: the role of mycorrhizal symbiosis. Functional Ecology 14: 397-399.

Tinker PB, Nye PH. 2000. Solute movement in the rhizosphere. Oxford, UK: Oxford University Press.

Veresoglou DS, Fitter AH. 1984. Spatial and temporal patterns of growth and nutrient uptake of five co-existing grasses. Journal ofEcology 72: 259-272.

van Vuuren MMI, Robinson D, Griffiths BS. 1996. Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant and Soil 178: 185 -192.

Wells CE, Eissenstat DM. 2001. Marked differences in survivorship among apple roots of different diameters. Ecology 82: 882-892.

van derWerfA, Kooijman A, Welschen R, Lambers H. 1988. Respiratory energy costs for the maintenance of biomass, for growth and for ion uptake in roots of Carex diandra and Carex acutiformis. Physiologia Plantarum 72: 483-491.

Wiesler F, Horst WJ. 1994. Root growth amd nitrate utilization of maize cultivars under field conditions. Plant and Soil 163: 267-277.

Wijesinghe DK, John EA, Beurskens S, Hutchings MJ. 2001. Root system size and precision in nutrient foraging: responses to spatial pattern of nutrient supply in six herbaceous species. Journal ofEcology 89: 972-983.

Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO. 2001.

Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiology 126: 875-890.

Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407-409.

Zhang H, Forde BG. 2000. Regulation of Arabidopsis root development by nitrate availability. Journal of Experimental Botany 51: 51-59.

Zhang H, Jennings A, Barlow PW, Forde BG. 1999. Dual pathways for regulation of root branching by nitrate. Proceedings of the National

Academy of Sciences, USA 96: 6529-6534.

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the plastic plant: root responses to heterogeneous supplies of nutrients

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